Cargando…

A bacterial filter protects and structures the gut microbiome of an insect

Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological...

Descripción completa

Detalles Bibliográficos
Autores principales: Lanan, Michele Caroline, Rodrigues, Pedro Augusto Pos, Agellon, Al, Jansma, Patricia, Wheeler, Diana Esther
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5029173/
https://www.ncbi.nlm.nih.gov/pubmed/26872040
http://dx.doi.org/10.1038/ismej.2015.264
_version_ 1782454474970759168
author Lanan, Michele Caroline
Rodrigues, Pedro Augusto Pos
Agellon, Al
Jansma, Patricia
Wheeler, Diana Esther
author_facet Lanan, Michele Caroline
Rodrigues, Pedro Augusto Pos
Agellon, Al
Jansma, Patricia
Wheeler, Diana Esther
author_sort Lanan, Michele Caroline
collection PubMed
description Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant (Cephalotes rohweri), blocking the entry of bacteria and particles ⩾0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral–rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host–microbe fidelity both during the animal life cycle and over evolutionary time.
format Online
Article
Text
id pubmed-5029173
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-50291732016-09-21 A bacterial filter protects and structures the gut microbiome of an insect Lanan, Michele Caroline Rodrigues, Pedro Augusto Pos Agellon, Al Jansma, Patricia Wheeler, Diana Esther ISME J Original Article Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant (Cephalotes rohweri), blocking the entry of bacteria and particles ⩾0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral–rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host–microbe fidelity both during the animal life cycle and over evolutionary time. Nature Publishing Group 2016-08 2016-02-12 /pmc/articles/PMC5029173/ /pubmed/26872040 http://dx.doi.org/10.1038/ismej.2015.264 Text en Copyright © 2016 International Society for Microbial Ecology http://creativecommons.org/licenses/by-nc-sa/4.0/ This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/
spellingShingle Original Article
Lanan, Michele Caroline
Rodrigues, Pedro Augusto Pos
Agellon, Al
Jansma, Patricia
Wheeler, Diana Esther
A bacterial filter protects and structures the gut microbiome of an insect
title A bacterial filter protects and structures the gut microbiome of an insect
title_full A bacterial filter protects and structures the gut microbiome of an insect
title_fullStr A bacterial filter protects and structures the gut microbiome of an insect
title_full_unstemmed A bacterial filter protects and structures the gut microbiome of an insect
title_short A bacterial filter protects and structures the gut microbiome of an insect
title_sort bacterial filter protects and structures the gut microbiome of an insect
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5029173/
https://www.ncbi.nlm.nih.gov/pubmed/26872040
http://dx.doi.org/10.1038/ismej.2015.264
work_keys_str_mv AT lananmichelecaroline abacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT rodriguespedroaugustopos abacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT agellonal abacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT jansmapatricia abacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT wheelerdianaesther abacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT lananmichelecaroline bacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT rodriguespedroaugustopos bacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT agellonal bacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT jansmapatricia bacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect
AT wheelerdianaesther bacterialfilterprotectsandstructuresthegutmicrobiomeofaninsect